INDUCTION OF APOPTOSIS IN CANCER CELLS BY PLANTS IN THE GENUS EUPHORBIA
DOI:
https://doi.org/10.14456/tbps.2018.15Keywords:
antiproliferative, cytotoxic, apoptosis, Euphorbia, cancerAbstract
Euphorbia is an evolutionarily distinct family of plants which have long been used in traditional medicine of diverse cultures to treat various ailments including cancer. In line with their traditional applications, research over the years has supported the anticancer properties of plants in the genus Euphorbia, particularly through their pro-apoptotic activities against various types of cancer cell lines. The aim of this review is to provide a summary of knowledge accumulated over the past few decades regarding the pro-apoptotic activities of the myriad euphorbia species, the chemical structure of isolated compounds and emerging pro-apoptotic mechanisms, as well as discussions relating to the future prospects for research and development of potential anticancer leads from plants in the genus Euphorbia.
References
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27. Han MH, Lee WS, Nagappan A, Kim HJ, Park C, Kim GY, et al. Polyphenols from Korean prostrate spurge Euphorbia supina induce apoptosis through the Fas-associated extrinsic pathway and activation of ERK in human leukemic U937 cells. Oncol Rep. 2016;36(1):99-107.
28. Fu ZY, Han XD, Wang AH, Liu XB. Apoptosis of human gastric carcinoma cells induced by Euphorbia esula latex. World J Gastroenterol. 2016;22(13):3564-72.
29. Hsieh WT, Lin HY, Chen JH, Kuo YH, Fan MJ, Wu RS, et al. Latex of Euphorbia antiquorum induces apoptosis in human cervical cancer cells via c-jun n-terminal kinase activation and reactive oxygen species production. Nutr Cancer. 2011;63(8):1339-47.
30. Hsieh WT, Lin HY, Chen JH, Lin WC, Kuo YH, Wood WG, et al. Latex of Euphorbia antiquorum-induced S-phase arrest via active ATM kinase and MAPK pathways in human cervical cancer HeLa cells. Environ Toxicol. 2015;30(10):1205-15.
31. Kim EJ, Park H, Park SY, Jun JG, Park JH. The grape component piceatannol induces apoptosis in DU145 human prostate cancer cells via the activation of extrinsic and intrinsic pathways. J Med Food. 2009;12(5):943-51.
32. Hsieh YJ, Chang CJ, Wan CF, Chen CP, Chiu YH, Leu YL, et al. Euphorbia formosana root extract induces apoptosis by caspase-dependent cell death via Fas and mitochondrial pathway in THP-1 human leukemic cells. Molecules. 2013;18(2):1949-62.
33. Fu Z, Han X, Du J, Han X, Liu W, Shao S, et al. Euphorbia lunulata extract acts on multidrug resistant gastric cancer cells to inhibit cell proliferation, migration and invasion, arrest cell cycle progression, and induce apoptosis. J Ethno-pharmacol. 2017;212:8-17.
34. Shekofteh N, Ghafourian Boroujerdnia M, Khosravi N, Kalantar K, Malek-Hosseini S, Namdari H, et al. Apoptosis-inducing Effect of the Hexane Extracts from Three Native Iranian Euphorbia Plants. Int J Cancer Manag. 2017;10(11): e8306.
35. Aghaei M, Yazdiniapour Z, Ghanadian M, Zolfaghari B, Lanzotti V, Mirsafaee V. Obtusifoliol related steroids from Euphorbia sogdiana with cell growth inhibitory activity and apoptotic effects on breast cancer cells (MCF-7 and MDA-MB231). Steroids. 2016;115:90-7.
36. Kwan YP, Saito T, Ibrahim D, Al-Hassan FM, Ein Oon C, Chen Y, et al. Evaluation of the cytotoxicity, cell-cycle arrest, and apoptotic induction by Euphorbia hirta in MCF-7 breast cancer cells. Pharm Biol. 2016;54(7):1223-36.
37. Luz LE, Kanunfre CC, Paludo KS, da Silva Justo A, Petry VK, Lemes BM, et al. Cytotoxic biomonitored study of Euphorbia umbellata (Pax) Bruyns. J Ethnopharmacol. 2016;183:29-37.
38. Amirghofran Z, Bahmani M, Azadmehr A, Javidnia K. Induction of apoptosis in leukemia cell lines by Linum persicum and Euphorbia cheiradenia. J Cancer Res Clin Oncol. 2006;132(7):427-32.
39. Zarei SM, Ayatollahi AM, Ghanadian M, Kobarfard F, Aghaei M, Choudhary MI, et al. Unusual ingenoids from Euphorbia erythradenia Bioss. with pro-apoptotic effects. Fitoterapia. 2013;91:87-94.
40. Duarte N, Ramalhete C, Varga A, Molnar J, Ferreira MJ. Multidrug resistance modulation and apoptosis induction of cancer cells by terpenic compounds isolated from Euphorbia species. Anticancer Res. 2009;29(11):4467-72.
41. Thafeni MA, Sayed Y, Motadi LR. Euphorbia mauritanica and Kedrostis hirtella extracts can induce anti-proliferative activities in lung cancer cells. Mol Biol Rep. 2012;39(12):10785-94.
42. Wang ZY, Liu HP, Zhang YC, Guo LQ, Li ZX, Shi XF. Anticancer potential of Euphorbia helioscopia L extracts against human cancer cells. Anat Rec (Hoboken). 2012;295(2):223-33.
43. Wang JH, Zhou YJ, Bai X, He P. Jolkinolide B from Euphorbia fischeriana Steud induces apoptosis in human leukemic U937 cells through PI3K/Akt and XIAP pathways. Mol Cells. 2011;32(5):451-7.
44. Xu HY, Chen ZW, Hou JC, Du FX, Liu JC. Jolkinolide B induces apoptosis in MCF-7 cells through inhibition of the PI3K/Akt/mTOR signaling pathway. Oncol Rep. 2013;29(1):212-8.
45. Lin Y, Cui H, Xu H, Yue L, Xu H, Jiang L, et al. Jolkinolide B induces apoptosis in MDA-MB-231 cells through inhibition of the PI3K/Akt signaling pathway. Oncol Rep. 2012;27(6):1976-80.
46. Wang Y, Ma X, Yan S, Shen S, Zhu H, Gu Y, et al. 17-hydroxy-jolkinolide B inhibits signal transducers and activators of transcription 3 signaling by covalently cross-linking Janus kinases and induces apoptosis of human cancer cells. Cancer Res. 2009;69(18):7302-10.
47. Yan SS, Li Y, Wang Y, Shen SS, Gu Y, Wang HB, et al. 17-Acetoxyjolkinolide B irreversibly inhibits IkappaB kinase and induces apoptosis of tumor cells. Mol Cancer Ther. 2008;7(6): 1523-32.
48. Lin MW, Lin AS, Wu DC, Wang SS, Chang FR, Wu YC, et al. Euphol from Euphorbia tirucalli selectively inhibits human gastric cancer cell growth through the induction of ERK1/2-mediated apoptosis. Food Chem Toxicol. 2012;50(12):4333-9.
49. Hoesel B, Schmid JA. The complexity of NF-kappaB signaling in inflammation and cancer. Mol Cancer. 2013;12:86.
50. Vander Heiden MG, Cantley LC, Thompson CB. Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science. 2009;324(5930): 1029-33.
51. Serova M, Ghoul A, Benhadji KA, Faivre S, Le Tourneau C, Cvitkovic E, et al. Effects of protein kinase C modulation by PEP005, a novel ingenol angelate, on mitogen-activated protein kinase and phosphatidylinositol 3-kinase signaling in cancer cells. Mol Cancer Ther. 2008;7(4):915-22.
2. Housman G, Byler S, Heerboth S, Lapinska K, Longacre M, Snyder N, et al. Drug resistance in cancer: an overview. Cancers. 2014;6(3):1769-92.
3. Ernst M, Grace OM, Saslis-Lagoudakis CH, Nilsson N, Simonsen HT, Ronsted N. Global medicinal uses of Euphorbia L. (Euphorbiaceae). J Ethnopharmacol. 2015;176:90-101.
4. Shi QW, Su XH, Kiyota H. Chemical and pharmacological research of the plants in genus Euphorbia. Chem Rev. 2008;108(10):4295-327.
5. Man S, Gao W, Wei C, Liu C. Anticancer drugs from traditional toxic Chinese medicines. Phytother Res. 2012;26(10):1449-65.
6. Ihsan ul H, Mirza B, Kondratyuk TP, Park EJ, Burns BE, Marler LE, et al. Preliminary evaluation for cancer chemopreventive and cytotoxic potential of naturally growing ethnobotanically selected plants of Pakistan. Pharm Biol. 2013;51(3):316-28.
7. de Melo JG, Santos AG, de Amorim EL, do Nascimento SC,
de Albuquerque UP. Medicinal plants used as antitumor agents in Brazil: an ethnobotanical approach. Evid Based Complement Alternat Med. 2011;2011:365359.
8. Mothana RA, Lindequist U, Gruenert R, Bednarski PJ. Studies of the in vitro anticancer, antimicrobial and antioxidant potentials of selected Yemeni medicinal plants from the island Soqotra. BMC Complement Altern Med. 2009;9:7.
9. Gartel AL. Mechanisms of apoptosis induced by anticancer compounds in melanoma cells. Curr Top Med Chem. 2012;12(1):50-2.
10. Kim R, Tanabe K, Uchida Y, Emi M, Inoue H, Toge T. Current status of the molecular mechanisms of anticancer drug-induced apoptosis. The contribution of molecular-level analysis to cancer chemotherapy. Cancer Chemother Pharmacol. 2002;50(5):343-52.
11. Zaman S, Wang R, Gandhi V. Targeting the apoptosis pathway in hematologic malignancies. Leuk Lymphoma. 2014;55(9):1980-92.
12. Elmore S. Apoptosis: a review of programmed cell death. Toxicol Pathol. 2007;35(4):495-516.
13. Green DR, Llambi F. Cell Death Signaling. Cold Spring Harb Perspect Biol. 2015;7(12).
14. Fallahian F, Ghanadian M, Aghaei M, Zarei SM. Induction of G2/M phase arrest and apoptosis by a new tetrahydroingenol diterpenoid from Euphorbia erythradenia Bioss. in melanoma cancer cells. Biomed Pharmacother. 2017;86:334-42.
15. Zhang JY, Huang WJ, Sun HM, Liu Y, Zhao XQ, Tang SL, et al. Structure Identification and In Vitro Anticancer Activity of Lathyrol-3-phenylacetate-5,15-diacetate. Molecules. 2017;22(9).
16. Lin M, Tang S, Zhang C, Chen H, Huang W, Liu Y, et al. Euphorbia factor L2 induces apoptosis in A549 cells through the mitochondrial pathway. Acta Pharm Sin B. 2017;7(1):59-64.
17. Liu M, Zhang W, Wang G, Song X, Zhao X, Wang X, et al. 13-Oxyingenol dodecanoate, a cytotoxic ingenol derivative, induces mitochondrial apoptosis and caspase-dependent Akt decrease in K562 cells. Tumour Biol. 2016;37(5):6227-38.
18. Bahmani B, Keyvanloo Shahrestanaki M, Ghanadian M, Hajiahmadi S, Aghaei M. Jatropha-6(17),11E-diene class derivatives induce apoptosis effects in OVCAR-3 and Caov-4 ovarian cancer cell lines via a mitochondrial pathway. Biochem Cell Biol. 2017:1-12.
19. Nabatchian F, Moradi A, Aghaei M, Ghanadian M, Jafari SM, Tabesh S. New 6(17)-epoxylathyrane diterpene: aellinane from Euphorbia aellenii induces apoptosis via mitochondrial pathway in ovarian cancer cell line. Toxicol Mech Methods. 2017;27(8):622-30.
20. Shen L, Zhang SQ, Liu L, Sun Y, Wu YX, Xie LP, et al. Jolkinolide A and Jolkinolide B Inhibit Proliferation of A549 Cells and Activity of Human Umbilical Vein Endothelial Cells. Med Sci Monit. 2017;23:223-37.
21. Gao C, Yan X, Wang B, Yu L, Han J, Li D, et al. Jolkinolide B induces apoptosis and inhibits tumor growth in mouse melanoma B16F10 cells by altering glycolysis. Sci Rep. 2016;6:36114.
22. Zhang JY, Liang YJ, Chen HB, Zheng LS, Mi YJ, Wang F, et al. Structure identification of Euphorbia factor L3 and its induction of apoptosis through the mitochondrial pathway. Molecules. 2011;16(4):3222-31.
23. Xu HY, Chen ZW, Li H, Zhou L, Liu F, Lv YY, et al.
12-Deoxyphorbol 13-palmitate mediated cell growth inhibition, G2-M cell cycle arrest and apoptosis in BGC823 cells. Eur J Pharmacol. 2013;700(1-3):13-22.
24. Fan L, Xiao Q, Chen Y, Chen G, Duan J, Tao W. Pekinenin E Inhibits the Growth of Hepatocellular Carcinoma by Promoting Endoplasmic Reticulum Stress Mediated Cell Death. Front Pharmacol. 2017;8:424.
25. Yang JL, Lien JC, Chen YY, Hsu SC, Chang SJ, Huang AC, et al. Crude extract of Euphorbia formosana induces apoptosis of DU145 human prostate cancer cells acts through the caspase-dependent and independent signaling pathway. Environ Toxicol. 2016;31(11):1600-11.
26. Cheng J, Han W, Wang Z, Shao Y, Wang Y, Zhang Y, et al. Hepatocellular carcinoma growth is inhibited by Euphorbia helioscopia L. Extract in Nude Mice Xenografts. Biomed Res Int. 2015;601015.
27. Han MH, Lee WS, Nagappan A, Kim HJ, Park C, Kim GY, et al. Polyphenols from Korean prostrate spurge Euphorbia supina induce apoptosis through the Fas-associated extrinsic pathway and activation of ERK in human leukemic U937 cells. Oncol Rep. 2016;36(1):99-107.
28. Fu ZY, Han XD, Wang AH, Liu XB. Apoptosis of human gastric carcinoma cells induced by Euphorbia esula latex. World J Gastroenterol. 2016;22(13):3564-72.
29. Hsieh WT, Lin HY, Chen JH, Kuo YH, Fan MJ, Wu RS, et al. Latex of Euphorbia antiquorum induces apoptosis in human cervical cancer cells via c-jun n-terminal kinase activation and reactive oxygen species production. Nutr Cancer. 2011;63(8):1339-47.
30. Hsieh WT, Lin HY, Chen JH, Lin WC, Kuo YH, Wood WG, et al. Latex of Euphorbia antiquorum-induced S-phase arrest via active ATM kinase and MAPK pathways in human cervical cancer HeLa cells. Environ Toxicol. 2015;30(10):1205-15.
31. Kim EJ, Park H, Park SY, Jun JG, Park JH. The grape component piceatannol induces apoptosis in DU145 human prostate cancer cells via the activation of extrinsic and intrinsic pathways. J Med Food. 2009;12(5):943-51.
32. Hsieh YJ, Chang CJ, Wan CF, Chen CP, Chiu YH, Leu YL, et al. Euphorbia formosana root extract induces apoptosis by caspase-dependent cell death via Fas and mitochondrial pathway in THP-1 human leukemic cells. Molecules. 2013;18(2):1949-62.
33. Fu Z, Han X, Du J, Han X, Liu W, Shao S, et al. Euphorbia lunulata extract acts on multidrug resistant gastric cancer cells to inhibit cell proliferation, migration and invasion, arrest cell cycle progression, and induce apoptosis. J Ethno-pharmacol. 2017;212:8-17.
34. Shekofteh N, Ghafourian Boroujerdnia M, Khosravi N, Kalantar K, Malek-Hosseini S, Namdari H, et al. Apoptosis-inducing Effect of the Hexane Extracts from Three Native Iranian Euphorbia Plants. Int J Cancer Manag. 2017;10(11): e8306.
35. Aghaei M, Yazdiniapour Z, Ghanadian M, Zolfaghari B, Lanzotti V, Mirsafaee V. Obtusifoliol related steroids from Euphorbia sogdiana with cell growth inhibitory activity and apoptotic effects on breast cancer cells (MCF-7 and MDA-MB231). Steroids. 2016;115:90-7.
36. Kwan YP, Saito T, Ibrahim D, Al-Hassan FM, Ein Oon C, Chen Y, et al. Evaluation of the cytotoxicity, cell-cycle arrest, and apoptotic induction by Euphorbia hirta in MCF-7 breast cancer cells. Pharm Biol. 2016;54(7):1223-36.
37. Luz LE, Kanunfre CC, Paludo KS, da Silva Justo A, Petry VK, Lemes BM, et al. Cytotoxic biomonitored study of Euphorbia umbellata (Pax) Bruyns. J Ethnopharmacol. 2016;183:29-37.
38. Amirghofran Z, Bahmani M, Azadmehr A, Javidnia K. Induction of apoptosis in leukemia cell lines by Linum persicum and Euphorbia cheiradenia. J Cancer Res Clin Oncol. 2006;132(7):427-32.
39. Zarei SM, Ayatollahi AM, Ghanadian M, Kobarfard F, Aghaei M, Choudhary MI, et al. Unusual ingenoids from Euphorbia erythradenia Bioss. with pro-apoptotic effects. Fitoterapia. 2013;91:87-94.
40. Duarte N, Ramalhete C, Varga A, Molnar J, Ferreira MJ. Multidrug resistance modulation and apoptosis induction of cancer cells by terpenic compounds isolated from Euphorbia species. Anticancer Res. 2009;29(11):4467-72.
41. Thafeni MA, Sayed Y, Motadi LR. Euphorbia mauritanica and Kedrostis hirtella extracts can induce anti-proliferative activities in lung cancer cells. Mol Biol Rep. 2012;39(12):10785-94.
42. Wang ZY, Liu HP, Zhang YC, Guo LQ, Li ZX, Shi XF. Anticancer potential of Euphorbia helioscopia L extracts against human cancer cells. Anat Rec (Hoboken). 2012;295(2):223-33.
43. Wang JH, Zhou YJ, Bai X, He P. Jolkinolide B from Euphorbia fischeriana Steud induces apoptosis in human leukemic U937 cells through PI3K/Akt and XIAP pathways. Mol Cells. 2011;32(5):451-7.
44. Xu HY, Chen ZW, Hou JC, Du FX, Liu JC. Jolkinolide B induces apoptosis in MCF-7 cells through inhibition of the PI3K/Akt/mTOR signaling pathway. Oncol Rep. 2013;29(1):212-8.
45. Lin Y, Cui H, Xu H, Yue L, Xu H, Jiang L, et al. Jolkinolide B induces apoptosis in MDA-MB-231 cells through inhibition of the PI3K/Akt signaling pathway. Oncol Rep. 2012;27(6):1976-80.
46. Wang Y, Ma X, Yan S, Shen S, Zhu H, Gu Y, et al. 17-hydroxy-jolkinolide B inhibits signal transducers and activators of transcription 3 signaling by covalently cross-linking Janus kinases and induces apoptosis of human cancer cells. Cancer Res. 2009;69(18):7302-10.
47. Yan SS, Li Y, Wang Y, Shen SS, Gu Y, Wang HB, et al. 17-Acetoxyjolkinolide B irreversibly inhibits IkappaB kinase and induces apoptosis of tumor cells. Mol Cancer Ther. 2008;7(6): 1523-32.
48. Lin MW, Lin AS, Wu DC, Wang SS, Chang FR, Wu YC, et al. Euphol from Euphorbia tirucalli selectively inhibits human gastric cancer cell growth through the induction of ERK1/2-mediated apoptosis. Food Chem Toxicol. 2012;50(12):4333-9.
49. Hoesel B, Schmid JA. The complexity of NF-kappaB signaling in inflammation and cancer. Mol Cancer. 2013;12:86.
50. Vander Heiden MG, Cantley LC, Thompson CB. Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science. 2009;324(5930): 1029-33.
51. Serova M, Ghoul A, Benhadji KA, Faivre S, Le Tourneau C, Cvitkovic E, et al. Effects of protein kinase C modulation by PEP005, a novel ingenol angelate, on mitogen-activated protein kinase and phosphatidylinositol 3-kinase signaling in cancer cells. Mol Cancer Ther. 2008;7(4):915-22.
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